RELATIONSHIP BETWEEN THE INTENSITY OF EXPOSURE TO MALARIA PARASITES AND INFECTION IN THE USAMBARA MOUNTAINS, TANZANIA

RENÉ BØDKER Danish Bilharziasis Laboratory, Charlottenlund, Denmark; National Institute of Medical Research, Amani, Tanzania; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom

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HAMISI A. MSANGENI Danish Bilharziasis Laboratory, Charlottenlund, Denmark; National Institute of Medical Research, Amani, Tanzania; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom

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WILLIAM KISINZA Danish Bilharziasis Laboratory, Charlottenlund, Denmark; National Institute of Medical Research, Amani, Tanzania; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom

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STEVE W. LINDSAY Danish Bilharziasis Laboratory, Charlottenlund, Denmark; National Institute of Medical Research, Amani, Tanzania; School of Biological and Biomedical Sciences, Durham University, Durham, United Kingdom

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The relationship between exposure to Plasmodium falciparum malaria and parasite density and prevalence was studied in six communities along an altitude transect. Prevalence of parasitemia in children decreased by 5% for every 100 meter increase in altitude from 82% in the lowlands at 300 meters to 12% in the highlands at 1,700 meters. This decrease in prevalence corresponded to a 1,000-fold reduction in transmission intensity. The ability to suppress parasite density and prevalence with age increased proportionally with increasing transmission intensity when transmission rates were higher than 0.1 infective bites per year, but developed after 2–3 years of age, regardless of transmission intensity. However, at transmission rates less than 0.1 infective bites per year, prevalence remained similar in all age groups. We propose that both exposure-dependent acquired immunity and age-dependent acquired immunity regulate parasite prevalence and density and suggest that transmission control will not hinder the development of protective anti-parasite immunity.

Author Notes

Reprint requests: René Bødker, Danish Institute for Food and Veterinary Research, Mørkhøj Bygade 19, 2860 Søborg, Denmark.
  • 1

    Trape J, Rogier C, 1996. Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 :236–240.

  • 2

    Snow RW, Nahlen B, Palmer A, Donnelly CA, Gupta S, Marsh K, 1998. Risk of severe malaria among African infants: direct evidence of clinical protection during early infancy. J Infect Dis 177 :819–822.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Metzger WG, Maxwell CA, Curtis CF, 1998. Anti-sporozoite immunity and impregnated bednets in Tanzanian villages. Ann Trop Med Parasitol 92 :727–729.

  • 4

    Askjaer N, Maxwell C, Chambo W, Staalsoe T, Nielsen M, Hviid L, Curtis C, Theander TG, 2001. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. Clin Diag Lab Immunol 8 :1289–1291.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Kariuki SK, Lal AA, Terlouw DJ, ter Kuile FO, Ong’echa JMO, Phillips-Howard PA, Orago ASS, Kolczak MS, Hawley WA, Nahlen BL, Shi YP, 2003. Effects of Permethrin-treated bed nets on immunity to malaria in Western Kenya II. Antibody responses in young children in an area of intense malaria transmission. Am J Trop Med Hyg 68 (Suppl 4):108–114.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Kariuke SK, ter Kuile FO, Wannemuehler K, Terlouw DJ, Kolczak MS, Hawley WA, Phillips-Howard PA, Orago ASS, Nahlen BL, Lal AA, Shi YP, 2003. Effects of permethrin-treated bed nets on immunity to malaria in Western Kenya I. Antibody responses in pregnant women and cord blood in an area of intense malaria transmission. Am J Trop Med Hyg 68 (Suppl 4):61–67.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Baird JK, 1995. Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today 11 :105–111.

  • 8

    McGregor IA, Wilson RJM, 1988. Specific immunity: acquired in man. Wernsdorfer WH, McGregor I, eds. Malaria. London: Churchill Livingstone, 559–619.

    • PubMed
    • Export Citation
  • 9

    Koella JC, 1991. On use of mathematical models of malaria transmission. Acta Trop 49 :1–25.

  • 10

    Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo , Masbar S, 1991. Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. Am J Trop Med Hyg 45 :65–76.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Baird JK, Purnomo, Basri H, Bangs MJ, Andersen EM, Jones TR, Masbar S, Harjosuwarno S, Subianto B, Arbani PR, 1993. Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. Am J Trop Med Hyg 49 :707–719.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Maxwell CA, Msuya E, Sudi M, Njunwa KJ, Carneiro IA, Curtis CF, 2002. Effect of community-wide use of insecticide-treated nets for 3–4 years on malaria morbidity in Tanzania. Trop Med Int Health 7 :1003–1008.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, Kuile FO, Hawley WA, Wannemuchler KA, Phillips-Howard PA, Rosen DH, Nahlen BL, Terlouw DJ, Adazu K, Vulule JM, Slutsker L, 2004. Sustainability of reductions in malaria transmission and infant mortality in Western Kenya with use of insecticide-treated bednets. JAMA 291 :2571–2580.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Eisele TP, Lindblade KA, Wannemuchler KA, Gimnig JE, Odhiambo F, Hawley WA, Kuile FO, Phillipd-Howard PA, Rosen DH, Nahlen BL, Vulule JM, Slutsker L, 2004. Effect of sustained insecticide-treated bed net use on all-cause child mortality in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 73 :149–156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, Lindsay SW, 2003. Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. J Med Entomol 40 :706–717.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Balls MJ, Bødker R, Thomas CJ, Kisinza W, Msangeni HA, Lindsay SW, 2004. Effect of topography on the risk of malaria infections in the Usambara Mountains, Tanzania. Trans R Soc Trop Med Hyg 98 :400–408.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Bendixen M, Msangeni HA, Pedersen BV, Shayo D, Bødker R, 2001. Diversity of Plasmodium falciparum populations and complexity of infections in relation to transmission intensity and host age: a study from the Usambara Mountains Tanzania. Trans R Soc Trop Med Hyg 95 :143–148.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    WHO, 1963. Terminology of Malaria. Geneva: World Health Organization.

  • 19

    Gilles HM, Warrell DA, 1993. Essential Malariology. Third edition. London: Hodder & Stoughton.

    • PubMed
    • Export Citation
  • 20

    Metselaar D, van Thiel PH, 1959. Classification of malaria. Trop Geogr Med 11 :157–161.

  • 21

    WHO, 1951. Report on the Malaria conference in Equatorial Africa. World Health Organ Tech Rep Ser 38 :1–72.

  • 22

    Lindsay SW, Bødker R, Malima R, Msangeni HA, Kisinza W, 2000. Effect of the 1997–98 El Niño on highland malaria in Tanzania. Lancet 355 :989–990.

  • 23

    Bagster Wilson D, 1949. Malaria incidence in central and south Africa. Boyd M, ed. Malariology. Philadelphia: W. B. Saunders Co, 800–810.

    • PubMed
    • Export Citation
  • 24

    Beier JC, Killeen GF, Githure JI, 1999. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg 61 :109–113.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Hay SI, Guerra CA, Tatem AJ, Atkinson PM, Snow RW, 2005. Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol 3 :81–90.

  • 26

    Boyd M, 1949. Malariology. Philadelphia: W.B. Saunders Company.

  • 27

    Ellman R, Maxwell CA, Finch R, Shayo D, 1998. Malaria and anaemia at different altitudes in the Muheza district of Tanzania: childhood morbidity in relation to level of exposure to infection. Ann Trop Med Parasitol 92 :741–753.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Greenwood BM, 1997. Malaria transmission and vector control. Parasitol Today 13 :90–92.

  • 29

    Pull JH, Grab B, 1974. A simple epidemiological model for evaluating the malaria inoculation rate and the risk of infection in infants. Bull World Health Organ 51 :507–516.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Nedelman J, 1985. Some new thoughts about some old malaria models. Math Biosci 73 :159–182.

  • 31

    Charlwood JD, Smith T, Lyimo E, Kitua AY, Masanja H, Booth M, Alonso PL, Tanner M, 1998. Incidence of Plasmodium falciparum infection in infants in relation to exposure to sporozoite-infected anophelines. Am J Trop Med Hyg 59 :243–251.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Boyd M, Kitchen SF, 1937. Observations of induced falciparum malaria. Am J Trop Med 17 :213–235.

  • 33

    Macdonald G, 1973. Dynamics of Tropical Disease. London: Oxford University Press.

    • PubMed
    • Export Citation
  • 34

    Bekessy A, 1976. Estimation of incidence and recovery rates of Plasmodium falciparum parasitemia from longitudinal data. Bull World Health Organ 54 :685–693.

  • 35

    Snow RW, Molyneux CS, Warn PA, Omumbo J, Nevill CG, Gupta S, Marsh K, 1996. Infant parasite rates and immunoglobin M seroprevalence as a measure of exposure to Plasmodium falciparum during a randomized controlled trial of insecticide-treated bed nets on the Kenyan coast. Am J Trop Med Hyg 55 :144–149.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Molineaux L, 1988. The epidemiology of human malaria as an explanation of its distribution, including some implications for its control. Wernsdorfer WH, McGregor I, eds. Malaria. London: Churchill Livingstone, 913–998.

    • PubMed
    • Export Citation
  • 37

    Dye C, Hasibeder G, 1986. Population dynamics of mosquito-borne disease: effects of flies which bite some people more frequently than others. Trans R Soc Trop Med Hyg 80 :69–77.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Stuyft P, Manirankunda L, Delacollette C, 1993. L’approche de risque dans le dianostic du paludrisme-maladie en regions d’altitude. Ann Soc Belg Med Trop 73 :81–89.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Gupta S, Snow RW, 1996. How do bednets influence the transmissibility of Plasmodium falciparum?Parasitol Today 12 :89–90.

  • 40

    Maxwell CA, Chambo W, Mwaimu M, Magago F, Carneiro IA, Curtis CF, 2003. Variation of malaria transmission and morbidity with altitude in Tanzania and with introduction of alphacypermetrin treated nets. Malar J 2 :28.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Curtis CF, Maxwell CA, Finch RJ, Njunwa KJ, 1998. A comparison of use of a pyrethroid either for house spraying or for bednet treatment against malaria vectors. Trop Med Int Health 3 :619–631.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Maxwell CA, Myamba J, Njunwa KJ, Greenwood BM, Curtis CF, 1999. Comparison of bednets impregnated with different pyrethroids for their impact on mosquitoes and on re-infection with malaria after clearance of pre-existing infections with chlorproguanil-dapsone. Trans R Soc Trop Med Hyg 93 :4–11.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Anderson RM, May RM, 1985. Herd immunity to helminth infection and implications for parasite control. Nature 315 :493–496.

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